Titi monkeys combine alarm calls to create probabilistic meaning

Abstract

Previous work suggested that titi monkeys Callicebus nigrifrons combine two alarm calls, the A- and B-calls, to communicate about predator type and location. To explore how listeners process these sequences, we recorded alarm call sequences of six free-ranging groups exposed to terrestrial and aerial predator models, placed on the ground or in the canopy, and used multimodel inference to assess the information encoded in the sequences. We then carried out playback experiments to identify the features used by listeners to react to the available information. Results indicated that information about predator type and location were encoded by the proportion of B-call pairs relative to all call pairs of the sequence (i.e., proportion of BB-grams). The results suggest that the meaning of the sequence is not conveyed in a categorical but probabilistic manner. We discuss the implications of these findings for current theories of animal communication and language evolution.

Fig. 1. Results of the multimodel inference analyses.

Circle colors in (A) to (C) refer to the Akaike’s weight, i.e., the probability that a given model supports the hypothesis (white: w = 0, weak support; red: w = 1, strong support; n.c.: the model did not converge). (A) Information encoded in titi monkey alarm sequences: Metrics are presented row-wise, and information hypotheses are presented column-wise. For simplicity, the null and urgency models were combined as “control,” and their weights were added. For the metric “probability that first call is A,” models that addressed the possibility that predator type and location were encoded are not relevant because the first call can only be one of two possibilities and, thus, can only provide information about predatory type or location. (B) Gaze reaction of titi monkeys to the information contained within the playback stimuli sequences, i.e., the original condition during which broadcasted sequences were recorded. For a graphic representation of the best model (interaction between predator type and location), see Fig. 2. (C) Gaze reaction of the titi monkey to the metrics extracted from the playback stimuli sequences. For a graphic representation of the best model (proportion of BB-grams), see Fig. 4. (D) Illustration of sequence metrics that support each hypothesis. Letters refer to the corresponding model weights in (A). (E) Illustration of experimental design of the predator presentations.

Fig. 2. Proportion of time the listener spent looking upward across original recording conditions of the playback stimuli.

The figure shows raw data (one line per individual), as well as estimates per condition (black circles) and bootstrapped estimates (colored circles, 1000 bootstraps) of the model testing how gaze reaction depends on both predator type and location (main effects). Subjects looked more upward when they were presented with sequences elicited by an aerial predator (compared to a terrestrial predator) or elicited by a predator in the canopy (as opposed to a predator on the ground). For simplicity, we displayed the most salient reaction, i.e., looking upward. Results for other looking directions can be found in fig. S2.

Fig. 3. Proportion of BB-grams in the alarm call response depending on the eliciting stimulus.

The figure shows estimates (black circles) and bootstrapped estimates per condition (colored circles, 1000 bootstraps) of the model testing how the proportion of BB-grams encodes both predator type and location (main effects). The proportion of BB-grams is higher in vocal responses to terrestrial predator than to aerial predators and higher when the predator is on the ground than when it is in the canopy.

Fig. 4. Listener’s gaze reaction, depending on the proportion of BB-grams of the alarm sequence.

Proportion of time listeners spent looking downward (A), toward the speaker (B), and upward (C), depending on the proportion of BB-grams of the playback stimuli. The figure shows raw data (circles), as well as estimates (black lines) and bootstrapped estimates (colored lines, 1000 bootstraps) of the model testing how gaze reaction depends on the proportion of BB-grams. Listeners spent more time looking toward the speaker (B) and less time looking upward (C) when there were more BB-grams in the sequence. The time looking downward (A) was not affected.